Colourful Orb-Weaving Spiders, Nephila Pilipes, Through a Bee's Eyes
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The Journal of Experimental Biology 207, 2631-2637 2631 Published by The Company of Biologists 2004 doi:10.1242/jeb.01068 Colourful orb-weaving spiders, Nephila pilipes, through a bee’s eyes I-Min Tso1, Chih-Wei Lin1 and En-Cheng Yang2,* 1Department of Biology, Tunghai University, Taichung 407, Taiwan and 2Department of Entomology, National Chung Hsing University, Taichung 402, Taiwan *Author for correspondence (e-mail: [email protected]) Accepted 4 May 2004 Summary Many orb-weaving spiders in the tropics forage in open reflectances of the background and body surface of sites during the day and some of them have both bright spiders showed that the brightly coloured body parts of and dark colourations. The conspicuous UV-reflective the typical morph exhibited rather high values, but those colour markings of these spiders have been reported to be of the dark body parts were below the discrimination attractive to visually oriented prey and thus could increase threshold. The differential colour contrasts of body parts the spiders’ foraging success. Using a combination of field generated a visual signal unlike that of a spider but rather and laboratory studies, we examine whether or not the like certain forms of food resources. On the other hand, body colouration of orb-weaving spiders exhibits optical the melanic morphs did not have bright colouration and properties that are attractive to insect prey from the the colour contrasts of every part of the body were viewpoint of insect visual physiology. We compared the significantly higher than the threshold, making the prey interception rates and colour contrasts of the typical contour of spiders quite clear to bees. and melanic morphs of the giant wood spider, Nephila pilipes. Results of the field study showed that the typical morph caught significantly more insects than the melanic Key words: colour contrast, visual signal, Apis mellifera, Nephila morph. Colour contrasts calculated from spectral pilipes, polymorphism. Introduction Various diurnal orb-weaving spiders in the tropics exhibit weaving spiders helped increase spiders’ foraging success by both bright and dark markings, and recently these bright being attractive to insects, it is still not clear how these markings markings have been considered to be important in predator–prey are perceived by prey and why they are attractive. visual interactions. Many spiders are active at night and their Many researchers attributed the attractiveness of spiders’ colourations are usually dark, grey or brown, to reduce the body colouration to the UV-reflecting properties. However, spiders’ visibility during daytime (Oxford and Gillespie, 1998). insects see by detecting the colour contrast between the objects However, some orb-weaving spiders of the families Araneidae they are looking at and the background of that object using a and Tetragnathidae forage during the day and many of them combination of several receptor signals (Chittka and Menzel, exhibit conspicuous colour patterns (Yaginuma, 1986). The 1992; Vorobyev and Brandt, 1997; Briscoe and Chittka, 2001). bright colour patterns of these diurnal orb-weaving spiders have Insects do not rely solely on UV signals but instead use light recently been proposed to be able to increase foraging success signals reflected from the objects and backgrounds for visual by providing attractive visual signals to prey. For example, the detection (Kevan et al., 2001). In the honeybee, chromatic brightly coloured dorsum of Argiope argentata in Panama was vision and achromatic vision are involved in the detection of demonstrated to be more attractive to insects than the spiders’ colour targets, depending on the subtended visual angle of the brown ventrum (Craig and Ebert, 1994). The spiny spiders target. While only contrast to the L (long-wavelength)-receptor Gasteracantha foricata in Australia also exhibit bright is used for detecting targets with subtending small visual colouration on their dorsum. Covering this colouration with angles (Giurfa and Vorobyev, 1998), the chromatic visual paint significantly reduced the spiders’ foraging success system of the honeybee, which receives input from all three (Hauber, 2002). The brightly coloured giant wood spider, photoreceptor types, is responsible for detecting targets with Nephila pilipes, in Asia caught significantly more insects than large visual angles (Giurfa et al., 1996, 1997; Niggebrügge and its melanic conspecifics, and the reason for this was suggested Hempel de Ibarra, 2003). Recently, the way in which to be the spiders’ ultraviolet (UV)-reflecting markings (Tso et hymenopteran insects perceive crab spiders (Family: al., 2002). However, even though these studies have all Thomisidae) on flowers was assessed by calculating the colour demonstrated that the brightly coloured markings of diurnal orb- contrasts derived from the reflectance spectra of the spiders and 2632 I.-M. Tso, C.-W. Lin and E.-C. Yang the petals (Chittka, 2001; Théry and Casas, 2002; Heiling et al., 2003). So far, this approach has not been used to assess the visual signals of diurnal 9 orb-weaving spiders. In the present study, we 4 10 examined how the colour markings of spiders 3 11 were viewed by insects, by measuring their 5 8 reflectance spectra, and then calculated the colour 2 7 12 contrasts as perceived by hymenopteran insects. 6 1 A polymorphic population of the giant wood spider, Nephila pilipes (formally N. maculata), on Orchid Island, Taiwan had been demonstrated previously to exhibit colour-associated foraging success (Tso et al., 2002). Typical morph female N. pilipes have an olive-green prosoma and a yellowish-black abdomen decorated with a Fig.·1. Schematic drawings illustrating the colour markings of the typical morph transverse white band, two longitudinal yellow giant wood spider Nephila pilipes. Reflectance spectra were recorded from the areas bands and numerous yellow spots (Fig.·1). specified (see Figs·5,·6). However, some of the females are totally dark, and allozyme data has demonstrated that both morphs are 5000–6000, 6000–7000, 7000–8000, 8000–9000 and members of an interbreeding population (Tso et al., 2002). A >9000·cm2. The Poisson model was expressed as: previous study on this population has shown that the typical log µ = log N(Xi) + Xiβ·, (1) morphs caught almost twice as much prey as the melanic N morphs (Tso et al., 2002). In the present study, we compared where µ was the expected value, Xi represented catching area the prey interception rates of two morphs of N. pilipes again or spider morphs, β was probability and N was total number to confirm whether or not a bright colouration will render a of individuals. higher foraging success. Moreover, we calculated the colour contrasts of these two morphs in the colour space of honey bees Measurements of light environment and spectral properties by measuring spectral reflectance of body surfaces and Reflectance spectra of the spiders, the background light background light environment in the study site to assess how environment and the illumination functions of the study sites these spiders are perceived by insects. were used to calculate the colour contrasts perceived by spiders’ prey and predators (Chittka et al., 1994). We measured the reflectance spectra of various objects with a spectrometer Materials and methods (S2000; Ocean Optics, Inc., Dunedin, FL, USA). In the study Field census of prey interception rate site, giant wood spiders usually hang their webs in the forest To examine whether the body colouration of Nephila pilipes understorey in front of dense vegetations. Therefore, the (Fabricus 1793) may provide an attractive signal to insects, background light environment was estimated by averaging the field censuses were conducted between 19 and 30 June 2002 reflectance spectra measured from green leaves, fallen leaves on Chung-Ai Bridge of Orchid Island (22°03′ N, 121°32′Ε), and bark (N=190 in total) collected from the field census site. Taitung County, Taiwan. Tso et al. (2002) give a detailed The daylight spectrum of the forest understorey illumination description of the study site. We marked the web sites of 18 was measured at the study site by placing the end of the probe typical and five melanic morphs of female N. pilipes by of the spectrometer 5·mm above (90°) the standard white. The fastening a tape on vegetation near by. Each day before measurements were taken every day at hourly intervals from 08.00·h, we measured the horizontal and vertical web 08.00·h to 18.00·h for three sunny days. The means of these diameters as well as the hub diameter of all marked webs. readings were used in the subsequent calculations of colour Catching areas of orbs were calculated by the ‘adjusted radii- contrasts. Eight typical and six melanic morphs were brought hub’ formula provided by Herberstein and Tso (2000). The to the laboratory to measure the reflectance spectra of various marked spiders were monitored once each hour each day areas on their body (Fig.·1). All the reflectance spectrum between 08.00·h and 18.00·h, and web damage, number and measurements in this study followed the standard procedures taxonomic order of prey caught by spiders were recorded. The described previously (Tso et al., 2002). The spectral reflectance prey interception data fitted well with a Poisson distribution measurements covered the range from 300·nm to 700·nm (Pearson χ2 test, P<0.05; Steel et al., 1997). Therefore, we used (increment 0.3·nm). For each wavelength, we measured the Poisson regression to examine the relationship between reflectance 10 times and we plotted the mean against the insect interception rate, catching area and spider morphs. wavelength. Categorical variables included catching area and spider Bees were reported to adopt achromatic vision by using the morphs. Catching areas were ranked according to the following green receptor signal when searching for objects far ahead and categories: <2000, 2000–3000, 3000–4000, 4000–5000, to adopt chromatic vision by using green, blue and UV receptor Colour contrast of spiders 2633 signals when approaching objects (Giurfa et al., 1997; Spaethe and y = EB – 0.5(EUV + EG)·, (6) et al., 2001).